Abstract
The formation of the musculoskeletal system is a remarkable example of tissue assembly. In both vertebrates and invertebrates, precise connectivity between muscles and skeleton (or exoskeleton) via tendons or equivalent structures is fundamental for movement and stability of the body. The molecular and cellular processes underpinning muscle formation are well-established and significant advances have been made in understanding tendon development. However, the mechanisms contributing to proper connection between these two tissues have received less attention. Observations of coordinated development of tendons and muscles suggest these tissues may interact during the different steps in their development. There is growing evidence that, depending on animal model and muscle type, these interactions can take place from progenitor induction to the final step of the formation of the musculoskeletal system. Here, we briefly review and compare the mechanisms behind muscle and tendon interaction throughout the development of vertebrates and Drosophila before going on to discuss our recent findings on the coordinated development of muscles and tendon-like structures in Drosophila leg. By altering apodeme formation (the functional Drosophila equivalent of tendons in vertebrates) during the early steps of leg development, we affect the spatial localization of subsequent myoblasts. These findings provide the first evidence of the developmental impact of early interactions between muscle and tendon-like precursors, and confirm the appendicular Drosophila muscle system as a valuable model for studying these processes.
Highlights
Genetics, Reproduction and Development Laboratory (GReD) Genetics, Reproduction and Development Laboratory, Institut National de la Santé et de la Recherche Médicale U1103, Centre National de la Recherche Scientifique UMR6293, Clermont University, Clermont-Ferrand, France
The data reported here show that in developing Drosophila legs, the invaginating tendon-like precursors orchestrate the spatial positioning of tightly associated appendicular founder myoblasts
This study demonstrates that appendicular myogenesis is an attractive model for studying early interactions between tendon-like and muscle progenitors
Summary
Drosophila muscles have to be properly attached to the (exo-)skeleton in order to transmit the force generated by fiber contraction. A low level of SrB isoform is required for induction of tendon-like precursors during early embryonic development (Becker et al, 1997; Vorbrüggen and Jäckle, 1997). These precursors secrete signaling molecules that are involved in muscle guidance and attachment. In a similar way to the craniofacial and limb tendons described in vertebrate studies, tendon-like precursors in Drosophila embryo are specified independently of muscle cells whereas the terminal phase of differentiation is muscle-dependent (Volk, 1999; Schnorrer and Dickson, 2004; Schweitzer et al, 2010)
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